Exogenous application of plant defense hormones alters the effects of live soils on plant performance
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Basic and Applied Ecology 56 (2021) 144 155 www.elsevier.com/locate/baae
Exogenous application of plant defense hormones alters the
effects of live soils on plant performance
Jing Zhanga,*, Klaas Vrielinga, Peter G.L. Klinkhamera, T.Martijn Bezemera,b
a
Institute of Biology Leiden (IBL), Leiden University, Sylviusweg 72, 2333 BE, Leiden, the Netherlands
b
Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, the Netherlands
Received 3 December 2020; accepted 20 July 2021
Available online 24 July 2021
Abstract
The overall effect of a live soil inoculum collected from nature on plant biomass is often negative. One hypothesis to explain
this phenomenon is that the overall net pathogenic effect of soil microbial communities reduces plant performance. Induced
plant defenses triggered by the application of the plant hormones jasmonic acid (JA) and salicylic acid (SA) may help to miti-
gate this pathogenic effect of live soil. However, little is known about how such hormonal application to the plant affects the
soil and how this, in turn, impacts plant growth. We grew four plant species in sterilized and inoculated live soil and exposed
their leaves to two hormonal treatments (JA and SA). Two species (Jacobaea vulgaris and Cirsium vulgare) were negatively
affected by soil inoculation. In these two species foliar application of SA increased biomass in live soil but not in sterilized
soil. Two other species (Trifolium repens and Daucus carota) were not affected by soil inoculum and for these two species
foliar application of SA reduced plant biomass in both the sterilized and live soil. Application of JA reduced plant biomass in
both soils for all species. We subsequently carried out a multiple generation experiment for one of the plant species, J. vulgaris.
In each generation, the live soil was a mixture of 10% soil from the previous generation and 90% sterilized soil and the same
hormonal treatments were applied. The negative effects of live soil on plant biomass were similar in all four generations, and
this negative effect was mitigated by the application of SA. Our research suggests that the application of SA can mitigate the
negative effects of live soil on plant growth. Although the inoculum of soil containing a natural live soil microbial community
had a strong negative effect on the growth of J. vulgaris, we found no evidence for an increase or decrease in negative plant-
soil feedback in either the control or the SA treated plants. Also plant performance did not decrease consistently with succeed-
ing generations.
© 2021 The Author(s). Published by Elsevier GmbH on behalf of Gesellschaft für Ökologie. This is an open access article
under the CC BY license (http://creativecommons.org/licenses/by/4.0/)
Keywords: Plant-soil interactions; Plant-soil feedback; Induced resistance; Rhizosphere soil; Salicylic acid; Jasmonic acid
Introduction ecological systems (Bever, 1994; Seipel, Ishaq & Menalled,
2019; Van der Heijden, Bardgett & van Straalen, 2008).
The interactions between plants and soil microorganisms Although the effects may vary depending on the plant spe-
have long been recognized for their importance in terrestrial cies and the soils tested, in the majority of cases the soil
microbial community has a negative effect on plant growth
(Kulmatiski, Beard, Stevens & Cobbold, 2008). Plants also
*Corresponding author.
E-mail address: j.zhang@biology.leidenuniv.nl (J. Zhang).
affect the composition of the soil microbial community,
https://doi.org/10.1016/j.baae.2021.07.011
1439-1791/© 2021 The Author(s). Published by Elsevier GmbH on behalf of Gesellschaft für Ökologie. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/)J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155 145 which, in turn, will impact plant growth. This process is communities that affect plant biomass. If the negative effect called plant-soil feedback (Bever, Westover & Antonovics, of the live soil (sterilized soil inoculated with a live soil 1997; van Breemen & Finzi, 1998). Most plant species microbial community) on plant biomass is caused by an exhibit negative conspecific soil feedbacks. This means that overall pathogenic effect, we expect that activating SA sig- they grow worse in soil, in which the same species has been naling in the plant by exogenous application mitigates the grown than in soil where other species have grown negative effects. As a result, we expect that the effects of SA (Kulmatiski et al., 2008). From natural situations and agri- application on plant biomass differ between plants in sterile culture, it is well-known that soil can become less suitable soil and in live soil. Exogenous application of JA typically for a species if this species is grown in the same soil for mul- induces resistance against herbivores and necrotrophic tiple generations. This negative effect is thought to be pathogens (Antico, Colon, Banks & Ramonell, 2012; caused by soil pathogens or root herbivores, allelopathy, Carvalhais, Schenk & Dennis, 2017; Palmer, Shang & Fu, nutrient immobilization or nutrient depletion (Miki, 2012). 2017; Pieterse, Leon-Reyes, van der Ent & van Wees, 2009; In some cases, plants also cause positive plant-soil feed- Van Dam & Oomen, 2008). JA signaling can exhibit nega- backs and these can be mediated by plants promoting rhizo- tive crosstalk with SA signaling (Leon-Reyes et al., 2010). bacteria, mycorrhizal fungi or other unknown mechanisms The responses of plants, after activating hormonal defense (Revillini, Gehring & Johnson, 2016; van der Putten, 2017). pathways, to an inoculum containing a live soil microbial Plant-induced resistance has been regarded as a promising community are, as yet, not well studied and understood. defense strategy against pathogens or herbivores (Haney & Moreover, the evidence for the existence of such effects is Ausubel, 2015; Lebeis et al., 2015; Yang, Ahammed, Wu, contradictory. Activation of JA and SA signaling pathways Fan, & Zhou, 2015). In nature, plants are exposed to com- did not affect the resident soil microflora in several studies plex selection pressures, involving both abiotic and biotic (Berendsen, Pieterse & Bakker, 2012; Doornbos, van Loon stresses. Plants are under constant attack by a myriad of & Bakker, 2012; Rashid & Chung, 2017), but a more recent pathogens and pests and have to compete with neighboring study showed that SA modulates colonization of the root plants. As a result, plants have evolved a wide range of microbiome by specific bacterial taxa (Lebeis et al., 2015). responses to cope with biotic stresses. The abilities of plants If the induction of signaling pathways in the plant leads to respond to different biotic stresses are regulated through to changes in the composition of the soil microbial com- sophisticated interacting hormonal signaling networks munity, its effect is likely to extend over time or plant (Arnaud & Hwang, 2015; Bezemer & van Dam, 2005; generations. Potentially this could lead to the selection of Fujita et al., 2006). Phytohormones are a group of natural more beneficial soil microbial communities either by sup- plant compounds with low molecular weights. Salicylic acid pressing pathogens or by promoting beneficial microbes. (SA), jasmonic acid (JA) and its methylated form MeJA, As far as we are aware, the effects of plant hormones ethylene (ET), abscisic acid (ABA), auxin, cytokinins through plants on soils containing a live microbial com- (CKs), gibberellins and brassinosteroids are commonly stud- munity over multiple generations have not been studied ied phytohormones. Plant hormones regulate many develop- so far, despite its potential to select for more beneficial mental and signaling networks. Although most hormones soils containing plant growth-promoting microbial com- have been implicated to be involved in defense pathways, munities in agriculture. the key regulator against pathogens and pests, are the phyto- In a preliminary experiment, we found strong evidence for hormones JA and SA (Bari & Jones, 2009). Experimental negative effects of soil that consisted of a mixture of 90% evidence indicates that application of SA to plant leaves, sterilized soil and 10% live soil on the growth of common activates systemic acquired resistance (SAR) against patho- ragwort (Jacobaea vulgaris), compared to sterilized soil. gens (Mandal, Mallick & Mitra, 2009; Reymond & After treating plants with SA, this negative effect dimin- Farmer, 1998). JA, in turn, activates induced defenses ished. Based on these findings, we grew four different plant against herbivores and necrotrophic pathogens species individually in both sterilized soil and live soil. (Nahar, Kyndt, de Vleesschauwer, H€ ofte & Gheysen, 2011). For J. vulgaris, the species that showed the strongest nega- Although to some extent, the SA or JA-induced hormonal tive effect towards the live soil, and for which this negative signaling pathway could interact with other phytohormones, effect was mitigated by foliar application of SA, we grew such as CKs, ET, ABA and auxins, they do show clear plants for three more generations. For each generation, ster- effects on the plant’s defense system when applied as single ilized soil was inoculated with live soil from the previous hormones (Berens et al., 2019; Fujita et al., 2006; generation from the same treatment. We addressed four Yang et al, 2015). questions: (1) Do the effects of live soil on plant biomass A still uncharted territory is how plant hormone-activated differ among plant species? (2) Does the foliar application signaling pathways impact soil microbial communities and of JA and SA alter the effects of the live soil on plant bio- how these, in turn, affect plant growth. Here we restricted mass for those species that were negatively affected by the ourselves to two prime hormones involved in activating live soil? (3) Does the negative effect of live soil change in defense pathways, SA and JA. We aimed to quantify the four successive generations of J. vulgaris for control plants effect of SA- or JA-induced resistance to the soil microbial and plants treated with SA or JA.
146 J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155
Materials and methods KNO3, 13.6 g KH2PO4, 49.2 g MgSO47H2O, 25.2 g
K2SO4, 2.24 g KOH and 3.29 g Fe-EDTA added to 1 liter
Plant material and seed germination demineralized water, and a stock solution with micro ele-
ments (a mixed solution of 0.181 g MnCl24H2O, 0.286 g
Jacobaea vulgaris (common ragwort), Cirsium vulgare H3BO3, 0.022 g ZnSO47H2O, 0.0078 g CuSO45H2O and
(bull thistle), Trifolium repens (white clover) and Daucus 0.0126 g NaMoO42H2O added to 1 liter demineralized
carota (wild carrot) were chosen because they are common water). Ten ml of each stock solution was diluted in 1 liter
native species in the dune area where we collected soil. We of demineralized water before use.
collected seeds at the dunes for J. vulgaris. C. vulgare, and The pots for each species were divided over six treat-
D. carota. T. repens seeds were bought from Cruydt-Hoeck, ments: two soil treatments (sterilized soil and live soil) and
a seed company that sells seeds of wild plant species (Nije- three hormonal treatments (JA, SA and control (only sol-
berkoop, The Netherlands). Prior to seed germination, all vent)). Each treatment was replicated 10 times. The experi-
seeds were shaken for 2 min in 70% ethanol, then washed ment, therefore, consisted of 240 pots (4 species £ 2 soil
with sterilized water, put for 12 min in 2% bleach, and treatments £ 3 (2 hormonal treatments and control) £ 10
finally rinsed four times with sterilized water to minimize replicates). The plant hormones JA and SA were applied
influences of seed-borne microbes. through foliar application three times a week for four conse-
cutive weeks. The first application was given when plants
were 14 days old. Either 0.75 § 0.05 ml of 100 mM JA or
Soil material SA was sprayed on the leaves while carefully avoiding spill-
over to the soil. The hormonal concentrations were chosen
The soil was collected at Meijendel, a calcareous sandy based on a previous research with J. vulgaris
area from a coastal dune area north of The Hague, The Neth- (Wei, Vrieling, Kim, Mulder & Klinkhamer, 2021). One
erlands (52 °11 N, 4 ° 31 ‘E). The topsoil was collected to a week later the treatment was repeated with 1.50 § 0.05 ml
depth of 15 cm after removing the grassland vegetation and of 100 mM JA or SA. In the next week, the treatment was
the organic layer of the surface. The soil was sieved using a repeated with 2.25 § 0.05 ml of 100 mM JA or SA. The JA-
5 mm mesh, homogenized with a concrete mixer, and then solution was prepared by adding 105.135 ml JA stock solu-
stored in 20-liter plastic bags (Nasco Whirl-Pak Sample tion to Milli-Q water until a final volume of 500 ml. The JA
Bag). Bags were either sterilized by 35-K Gray gamma-irra- stock solution was prepared by adding 500 mg JA to 5 ml
diation (Synergy Health Company, Ede, The Netherlands) ethanol. JA was purchased from Cayman Chemical Com-
or kept at 4 C for inoculation. pany (product number: 88,300). SA solution (purchased
from Sigma-Aldrich, 99.0%) was made by dissolving
6.9055 mg in 69.055 ml of ethanol to which Milli-Q water
Plant growth and foliar application of hormones was added until a final volume of 500 ml. Control plants
were sprayed with sterile water with the same solvent (85 ml
Surface-sterilized seeds of the four species (J. vulgaris, C. ethanol in 500 ml Milli-Q water).
vulgare, T. repens and D. carota) were germinated in sterile
Petri dishes on filter paper. After one week, 60 seedlings per
species were planted individually in 500 ml pots containing Harvesting plants and soil samples
either sterilized soil or inoculated live soil. The live soil con-
sisted of a mixture of 90% sterilized soil and 10% live soil. Fifty-four days after planting, all plants were harvested,
Nutrient availability often increases after sterilization of the except for C. vulgare. C. vulgare plants were considerably
soil, and we therefore inoculated the sterilized soil rather larger than the other species and were therefore harvested
than using pure live soil, to enable comparison of the two after 45 days to prevent pot size limiting growth. Plants
types of soil. Sterilized soil and live soil were kept in bags were gently removed from the pots. Shoots were separated
and left in the climate room for 14 days to enable the estab- from roots with a scissor just above the root crown, and
lishment of microbial communities in the inoculated soil roots were rinsed with water and then put into paper bags.
before potting. Before potting, the soil in each bag was Harvested plant parts were oven-dried at 60 C for approxi-
mixed. After planting the seedlings, pots were randomly dis- mately one week. The dry weight of roots and shoots was
tributed over a climate room (relative humidity 70%, light determined to the nearest 0.1 mg. The rhizosphere soil was
16 h at 20 C, dark 8 h at 20 C). Plants were watered regu- harvested individually from each pot by gently shaking the
larly with Milli-Q water. Five ml Steiner nutrient solution roots and soil three times to remove the loosely adhering
was added per plant on day 7. Ten ml Steiner nutrient solu- soil, after which rhizosphere soil samples were collected
tion was added on day 13, and 20 ml Steiner nutrient solu- onto a sterile filter paper by removing the remnant soil from
tion was added on days 19, 28, 37 and 42. The Steiner the roots with a fine sterilized brush. Finally, all the labeled
nutrient solution (Steiner, 1979) was prepared from seven soil samples were transferred to a 4 C room and stored for
different stock solutions (106.2 g Ca(NO3)24H2O, 29.3 g the multiple generation experiment.J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155 147 Multi-generation experiment Statistical analysis J. vulgaris was chosen for the multiple generation selec- Data were first checked for homogeneity of variance (Lev- tion experiment to examine if the observed effect on plant ene's test) and normal distribution (Shapiro Wilks) of errors biomass of the first generation would increase further over and data were transformed when necessary. To test whether later generations. The soil for the multi-generational J. vul- the effect of the live soil was different among the four species garis experiment was derived from the pots from the previ- we performed a three-way ANOVA on the total data set of ous generation of J. vulgaris plants. For J. vulgaris we grew the first experiment with soil (sterilized and live, 2 levels), the plants from each of the six treatments (sterilized and live hormones (3 levels) and species (4 levels) as fixed factors. soils, two hormone treatments and control) for another three Live-soil responsiveness was used as a dependent variable generations under the same conditions as described for the and was arcsine square-root transformed prior to analysis first generation. The only difference being that each time, (Rowe, Brown & Claassen, 2007). Live-soil responsiveness the soil inoculum was derived from the previous generation was calculated as 100 times the dry mass of a plant divided from the same treatment, 100% sterilized soil was used as by the average dry mass of the control plants from the same control. A schematic drawing of the experiment is presented species in the sterilized soil. In this way, the average dry mass in Fig. 1. Fourteen days after mixing the sterilized and live of the control plants in the sterilized soil was set to 100 for soil, a single J. vulgaris seedling was planted into each pot. each of the four species. By doing so we removed species- All replicate rhizosphere soils from a single treatment were specific size differences to make the data more comparable mixed before inoculation to avoid a selection of particular among species. This analysis showed a significant microbial species in individual pots. All treatments were car- soil £ species interaction (results section). On the basis of ried out as described above. this we divided the data set in two groups. One group for the Fig. 1. Experimental design of the multigenerational experiment with J. vulgaris. Soil used for the 1st generation was a mixture of 90% steril- ized soil and 10% live soil both collected from the dunes. Soil used for the 2nd, 3rd and 4th generations was a mixture of 10% rhizosphere soil collected from the previous generation from the same treatment and 90% sterilized soil collected from the dunes. In each generation plants were grown for six weeks and all seeds were derived from the same batch of seeds. In each generation we tested two hormonal treatments in inoculated and 100% sterilized soil. JA denotes foliar application of jasmonic acid, SA denotes foliar application of salicylic acid and C denotes control. In each treatment 10 replicates were used even though only three are depicted.
148 J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155 two species that were negatively affected by the lives soil and dependent variable and generation was the independent vari- one group for the two species that were not. We did this able. Since we could not pair the pots (SA or JA/control) and because we expected the effect of the hormonal treatments to we only had 10 replicates for each treatment, we used a be only present for the species that were affected by live soil. Monte-Carlo simulation to test if the linear regression model To answer the question if the effect of the live soil was differed from y = 1. Each time we randomly paired one plant affected by foliar application of hormones we performed four of the hormone treatment and one plant of the control to cal- three-way ANOVAs (for the two groups of species and the culate the ratio of the dry mass of treated and dry mass of two hormonal treatments) with plant mass as dependent vari- control. Then we repeated this procedure 1000 times, to able and species (2 levels), soil (2 levels) and hormonal treat- obtain 1000 ratios of each generation per soil. Then we took ment (2 levels) as fixed factors. Usually, the negative effects the mean of 1000 ratios per generation to fit linear regression of live soil on plant biomass are stronger in the roots than the models for the two soils, respectively. To test whether the shoots, thus we also carried out three-way ANOVA analysis linear regressions in sterilized and live soils differed from for shoot-root ratios of the four plant species. y = 1, we calculated the 95% confidence intervals (CFI) of To answer the question whether the negative effect of live the slopes for both soils. We also tested whether the two lin- soil changes in four successive generations of J. vulgaris for ear regression models differed between sterilized and live control plants and plants treated with SA or JA we used a soils with ANCOVA (analysis of covariance) analysis. All three-way ANOVA with soil (2 levels), generation (4 levels) analyses were performed in IBM SPSS Statistics 25. and hormones (3 levels) as fixed factors, and log-trans- formed plant dry mass or shoot-root ratio as dependent vari- ables. We furthermore compared the effects of the two Results hormones separately using a three-way ANOVA with log- transformed plant dry mass as a dependent variable and soil Do the effects of live soil on plant biomass differ (2 levels), hormone (2 levels) and generation (4 levels) as among plant species? fixed factors. Differences between treatments were tested with a Tukey post-hoc test. For J. vulgaris and C. vulgare, biomass in live soils was We used a linear regression model to estimate the effects about half that in sterilized soils. This negative effect of the of SA and JA on the growth of J. vulgaris over four conse- live soil was present irrespective of the hormonal treatment. cutive generations in both sterilized and live soil. In the For the other two species (T. repens and D. carota) biomass regression model, the dry mass of plants of the SA or JA was not significantly different in live and sterilized soils treatments divided the dry mass of control plants was the (Fig. 2, Table 1). The difference in response to live soils Fig. 2. Mean (+ SE) responsiveness (%) of J. vulgaris, C. vulgare, T. repens and D. carota plants treated with JA and SA in sterilized soil and live soil. Responsiveness is dry mass of a treated plant divided by the average dry mass of the control plants in sterilized soil *100. C repre- sents control. Note: within species different letters above bars indicate significant differences between treatments based on a Tukey post-hoc test for each single species.
J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155 149
Table 1. Three-way ANOVA of arcsine square-root transformed the differences between the SA treatment and the control
responsiveness of J. vulgaris, C. vulgare, T. repens and D. carota were not significant (Fig. 2), the effect of the SA treatment,
in live and sterilized soil for plants treated with JA or SA and for as we hypothesized, depended strongly on soil type as is
control plants. df = degrees of freedom. reflected by the significant soil £ hormone interaction term
in the ANOVA (Table 2). For the two species (T. repens, D.
Source of variation df F-value P
carota) that were not negatively affected by the live soil,
Species 3, 239 53.67 *** foliar application of SA reduced plant biomass in both soils,
Soil 1, 239 147.78 *** although this effect was not significant (Fig. 2, Table 2).
Hormone 2, 239 27.17 ***
Species £ Soil 3, 239 59.81 ***
Species £ Hormone 6, 239 0.45 ns
Soil £ Hormone 2, 239 4.75 **
SP £ S £ H 6, 239 1.48 ns
Jasmonic acid
**
P < 0.01,. Foliar application of JA decreased plant mass in all plant
***
P < 0.001, ns not significant. species in both sterilized and live soils. For the two species
that were negatively affected by live soil the negative effect
among the four species is reflected by the highly significant of JA was stronger in sterilized soil than in live soil (Fig. 2).
interaction term (species £ soil) in the ANOVA (Table 1). This difference in response between plants grown in the two
Does the foliar application of JA and SA alter the effects soils was significant as reflected by the soil £ hormone
of live soil on plant biomass for those species that were neg- interaction term in the ANOVA (Table 2). For the two spe-
atively affected by live soil? cies that did not grow less well in the live soils, such a differ-
ence in the response to JA application in the two soils was
not found (Table 2).
Salicylic acid The shoot-root ratio of plants differed among species,
soils and hormone treatments (see Appendix A: Table S1).
For the two species (J. vulgaris and C. vulgare) that were Except for T. repens, JA application increased the shoot-
negatively affected by the live soil, foliar application of SA root ratio. We found no significant effects of SA application
reduced the biomass of plants grown in the sterilized soil on the shoot-root ratio. The effects of hormone application
while it increased the biomass of plants grown in the live on the shoot-root ratio varied among species and soils. In all
soil (Fig. 2). As a result, the main effect of SA in the species, the shoot-root ratio was, on average, higher in live
ANOVA was not significant (Table 2). Although by itself soils (See Appendix A: Fig. S1).
Table 2. Three-way ANOVAs of arcsine square-root transformed responsiveness for species that grew less well in live soil compared to ster-
ilized soil (upper part) and for species that were not negatively affected by the live soil (lower part). Left: hormonal treatment is foliar applica-
tion of SA. Right: hormonal treatment is foliar application of JA. Species, soil (live or sterilized), and hormone treatment were used as fixed
factors. df = degrees of freedom.
SA treatment JA treatment
Species respond to soil effect Source of variation Df F-value P df F-value P
Yes Species 1, 79 10.00 * 1, 79 5.25 *
(J. vulgaris Soil 1, 79 190.26 ** 1, 79 191.88 ***
C. vulgare) Hormone 1, 79 2.87 ns 1, 79 21.04 ***
Species £ Soil 1, 79 11.17 ** 1, 79 12.57 **
Species £ Hormone 1, 79 0.35 ns 1, 79 0.08 ns
Soil £ Hormone 1, 79 8.20 ** 1, 79 8.49 **
SP £ S £ H 1, 79 0.05 ns 1, 79 0.00 ns
No Species 1, 79 7.56 ** 1, 79 5.74 *
(T. repens Soil 1, 79 0.92 ns 1, 79 1.97 ns
D. carota) Hormone 1, 79 0.35 ns 1, 79 32.94 ***
Species £ Soil 1, 79 0.48 ns 1, 79 0.36 ns
Species £ Hormone 1, 79 1.10 ns 1, 79 1.86 ns
Soil £ Hormone 1, 79 1.21 ns 1, 79 1.58 ns
SP £ S £ H 1, 79 0.08 ns 1, 79 1.44 ns
P < 0.05,
*
**
P < 0.01,
***
P < 0.001, ns not significant.150 J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155
Fig. 3. Mean (+ SE) plant dry mass of J. vulgaris during four successive generations treated with JA and SA in sterilized soil and live soil. C
represents control. For each generation soil from the previous generation and originating from the same treatment was used as an inoculum.
Within each generation, different letters above bars indicate significant differences between groups based on a Tukey post-hoc test.
Does the negative effect of live soil change in four succes- generations in live soils while it was close to 1 in sterilized
sive generations of J. vulgaris for control plants and plants soils. This difference between the two soils was significant
treated with SA or JA? (ANCOVA df = (1, 7), F = 20.18, P < 0.01, Fig. 4A). The
slopes of the regressions for both sterilized and live soils did
not significantly differ from 0 (for sterilized soil the lower
The effect of the live soil across generations and upper 95% CFIs are 0.15 and 0.19; for live soil the
lower and upper 95% CFIs are -0.13 and 0.33). The latter
As in generation 1, in all three subsequent generations results indicate that there is no significant trend in the effect
plants grew less well in live soil than in sterilized soil. of foliar application of SA over generations.
Although the strength of this effect varied among genera-
tions there was no clear trend across subsequent generations
(Fig. 3, Table 3). The effect of foliar application of JA across
generations
The effect of foliar application of SA across As in generation 1, in all three subsequent generations
generations foliar application of JA reduced plant biomass in both steril-
ized and live soil (Fig. 3, Table 4). This reduction was less
Again as in generation 1, in all three subsequent genera- strong in live soil, as is reflected by the significant soil x hor-
tions foliar application of SA reduced plant biomass in steril- mone interaction term in the ANOVA (Table 4). The effect
ized soil and increased plant biomass in live soils (Fig. 3, of foliar JA application did not differ among generations as
Table 4). Although within generations and soils these differ- was reflected by the non-significant interaction term in the
ences were not significant, plants responded clearly differ- ANOVA (Table 4). To examine if the effect of JA applica-
ently to the SA treatment in the two soils as is reflected by tion in live and sterilized soils showed a trend over genera-
the significant soil £ hormone interaction term in the tions in more detail, we regressed the ratio between the dry
ANOVA (Table 4). The effect of foliar SA application did mass of JA-treated and control plants in both sterilized and
not differ among generations as was reflected by the non- live soils against generations (Fig. 4B). This ratio was lower
significant interaction term in the ANOVA (Table 4). To than 1 for all generations in both live soils and sterilized
examine if the effect of hormone application in live and ster- soils. The ratios did not differ between the two soils
ilized soil showed a trend over generations in more detail, (ANCOVA df = (1, 7), F = 0.01, P > 0.05, Fig. 4B). The lat-
we regressed the ratio between the dry mass of SA-treated ter result is somewhat surprising given the significant inter-
and control plants in both sterilized and live soils against action we found between the effects of JA application and
generations (Fig. 4). This ratio was higher than 1 for all soil type in Table 4. The slopes of the regressions for bothJ. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155 151
Table 3. Three-way ANOVA of log-transformed plant dry mass of sterilized and live soils did not significantly differ from 0
J. vulgaris during four generations in live and sterilized soils after (for sterilized soil the 95% CFI is 0.31 to 0.21; for live soil
JA, SA treatments and control. df = degrees of freedom. the 95% CFI is 1.8 to 0.24). The latter results indicate that
there is no significant trend in the effect of foliar application
Source of variation df F-value P of JA over generations.
Soil 1, 250 569.88 *** The shoot-root ratio of J. vulgaris differed among genera-
Hormone 2, 250 39.83 *** tions and was affected by soil and hormone treatments (See
Generation 3, 250 68.36 *** Appendix A: Table S2). While the effects of hormone appli-
Soil £ Hormone 2, 250 8.17 *** cation on the shoot-root ratio did not vary among genera-
Soil £ Generation 3, 250 57.96 *** tions, the effects of the hormone treatments differed among
Hormone £ Generation 6, 250 1.88 ns soils. In general, in both sterilized and live soils, application
S£H£G 6, 250 0.68 ns of JA increased shoot-root ratios relative to the control and
***
P < 0.001, ns not significant. the SA treatments except for the third generation in live soil
(See Appendix A: Fig. S2). Application of SA did not affect
Table 4. Three-way ANOVAs of plant dry mass of J. vulgaris during four generations in live and sterilized soils with soil (live and sterilized
soils), generation, hormone (control and SA, or control and JA) as fixed factors. df = degrees of freedom.
SA treatment JA treatment
Source of variation df F-value P df F-value P
Soil 1, 164 241.79 *** 1, 170 307.05 ***
Hormone 1, 164 0.28 ns 1, 170 39.11 ***
Generation 3, 164 8.98 *** 3, 170 11.07 ***
Soil £ Hormone 1, 164 8.75 ** 1, 170 11.36 **
Soil £ Generation 3, 164 7.98 *** 3, 170 7.12 ***
Hormone £ Generation 3, 164 0.17 ns 3, 170 0.14 ns
S£H£G 3, 164 0.50 ns 3, 170 0.70 ns
**
P < 0.01,.
***
P < 0.001, ns not significant.
Fig. 4. The ratio of dry mass of hormone-treated J. vulgaris plants divided by control plants in both sterilized and live soil for four genera-
tions. (A) SA-treated plants (B) JA-treated plants. C represents control. The dashed line indicates y = 1. The data points are the average of
1000 ratios of dry mass of SA or JA and dry mass of control for each generation, the error bars represent the 95% confidence intervals of
1000 ratios for each generation (see material and methods for details).152 J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155
the shoot-root ratio across generations in the sterilized and live soil. These results strongly suggest that the negative
live soils. impact of the live soil on plant biomass is driven by patho-
gens. T. repens and D. carota were unresponsive to the soil
with a live soil inoculum. The difference in response
between the four species can have different non-exclusive
Discussion
causes. The pathogenic effect of the live soils itself may dif-
fer among plant species due to specificity of the soil micro-
In this study, we examined how exogenous application of
bial species in the live soil inoculum, or due to inherent
the plant signaling hormones SA and JA interacts with the
plant characteristics. We started with our hormone applica-
effects of inoculation of soil on plant biomass of different
tion when seedlings were 14 days old. In retrospect, we
plant species and how those effects altered plant perfor-
should have started earlier. The negative effects of the live
mance during multiple consecutive generations. In two of
soil on plant biomass are most apparent during the first few
the four species, plant biomass was lower in live soil than in
weeks of plant growth (Bezemer, Jing, Bakx-Schotman &
sterilized soil. We found that foliar application of SA miti-
Bijleveld, 2018). If we would have applied the exogenous
gated the negative effects of the live soil on plant perfor-
SA earlier, effects may therefore have been stronger because
mance for these species. We then grew J. vulgaris for three
plants in our study may have outgrown the negative effects
additional generations and found that SA application miti-
of the live soil e.g. by upregulating their defense system
gated the negative effect of live soil on plant biomass in all
(Metrauxs, 2001; Netherway, Bengtsson, Krab, & Bahram,
four generations, and that this overall effect was significant.
2020; Vernooij et al., 1994). In addition, in this paper, we
used only one concentration of the phytohormones. Plant
species may have a different sensitivity to the foliar applica-
The response of plant species to live soil is species-
tion of these hormones, and the species that did not show a
specific
response may have responded to higher concentrations. It is
important to note that, in this paper, we performed experi-
Our results show that the effect of live soil on plant bio-
ments with two phytohormones. Other plant hormones like
mass strongly varied among plant species, although all
auxins and cytokinins have been reported to play a role in
plants received the same soil inoculum containing a natural
fighting off the potentially pathogenic bacteria in the live
soil microbial community and the growth conditions were
soil via changing physiological and morphological features
identical for all four species. Species-specific effects have
of plants (Clarke, Burritt, Jameson & Guy, 2000; Ham-
also been found in other plant-soil feedback experiments,
ill, 1993). They may interact with JA or SA signaling path-
which showed that J. vulgaris and C. vulgare responded
ways, however, this is still not fully understood. Applying
negatively to soil conditioning by conspecifics, while this is
combinations of different phytohormones would present a
not clear for T. repens and D. carota (Harrison & Bard-
next logical step. To find a clear effect of SA and JA on
gett, 2010; Joosten, Mulder, Klinkhamer & van Veen, 2009;
plant biomass against the pathogenic effect caused by live
Klironomos, 2002; Wang et al., 2019). Together these
soils is the base for carrying out more extensive experi-
results show that the responses of plant species to live soil
ments. For example, in further tests, different plant hor-
are highly species-specific. Other studies have suggested
mones and their crosstalk effects could be tested.
that net positive or negative plant-soil feedback effects are
related to the capacity of plants to cope with biotic or abiotic
stresses, to influence soil nutrients, or to the way they impact
soil microbial communities (Bezemer et al., 2006; De Long
Foliar application of SA mitigates the negative live
et al., 2019; Eisenhauer et al., 2011; Van der Heijden et al.,
soil effect on J. vulgaris
2008). The soil microbial community present in live soil
might have pathogenic effects on plant growth. This is in
Importantly, application of SA mitigated the negative
line with previous studies that indicate that soil sterilization
effects of the live soil on the growth of J. vulgaris in all four
enhanced plant biomass by killing soil-borne pathogens in
generations. Sterilization of the soil resulted in higher plant
crops (Li et al., 2019).
biomass, indicating an overall pathogenic effect due to soil-
borne pathogens, and SA-induced resistance may help to
mitigate this pathogenic effect caused by soil pathogens.
The response of plant species to SA application is Activation of SA-dependent signaling pathways lead to the
species-specific expression of pathogenesis-related proteins (PRP) contribut-
ing to resistance, by limiting pathogen growth, the access of
The effect of SA application also varied among plant spe- pathogens to water and nutrients in the plant, or by changing
cies. Interestingly, a positive effect of SA on plant biomass the composition of the cell wall of the plant (Glaze-
in live soils occurred in J. vulgaris and C. vulgare, J. vulga- brook, 2005; Heil & Bostock, 2002; O'Donnell, Jones,
ris and C. vulgare responded negatively to exposure to the Antoine, Ciardi & Klee, 2001; Spoel, Johnson & Dong,J. Zhang et al. / Basic and Applied Ecology 56 (2021) 144 155 153
2007). All this can result in higher plant mass in SA-treated Conclusions
plants than in control plants in live soil. In addition, activa-
tion of the SA pathway regulates a myriad of enzymes, for Overall, our study suggests that negative effects in live
example, peroxidase (POD), polyphenol oxidase (PPO), soil on plant biomass can be mitigated with foliar applica-
superoxide dismutase (SOD). Those enzymes play an tions of SA. Sterilization benefited plant biomass for two of
important role in plant SA-induced defense against biotic the four species we investigated, suggesting the microbial
stresses caused by pathogens (Achuo, Audenaert, Meziane community in live soils contains pathogens. For J. vulgaris,
& H€ofte, 2004; Bakker, Chaparro, Manter & Vivanco, the plant species that responded most strongly to SA appli-
2015; War, Paulraj, War & Ignacimuthu, 2011). The effects cation, we did not observe an increasingly stronger effect on
of SA in the first generation were similar to those observed plant biomass over further plant generations, but instead, the
in the second or later generations indicating that SA applica- effect was stable over time. To better understand what
tion did not select for less pathogenic or more beneficial soil caused the positive effect of SA application on plant bio-
microbial communities over time. The soil microbial com- mass in live soil, the changes in the diversity and functional
munity present in live soil might have pathogenic effects on role of the soil microbial community in live soil should be
plant biomass and this is related to the accumulation of examined in future studies.
pathogens across generations (Li, Ding, Zhang & Wang,
2014), however, we did not find a significant decrease in
biomass over generations. In part, this may be an artefact of Funding
the experimental set-up. For each generation, we used an
inoculum, which means that we placed a subset of the This research did not receive any specific grant from
microbial community in a sterile background. This may funding agencies in the public, commercial, or not-for-profit
have led to selection for microbes with characteristics in sectors.
each of the four generations. However, we urge not to over-
emphasize the conclusion that application of SA results in a
change in the effects of live soils on plant biomass over gen- Declaration of Competing Interest
erations. Future studies should also include a comparison
between the growth of SA-treated plants and control plants None
grown in soils that are conditioned by either SA-treated
plants and control plants in a full factorial design.
Acknowledgments
We would like to thank Karin van der Veen-van Wijk for
Foliar application of hormones affected plants assistance at the final biomass harvest, Jan Vink for driving
us to the field site to collect soil used for the inoculation
JA-induced defenses are activated in response to herbi-
experiment, Gang Chen for collecting soil and the China
vore attack, the infection of necrotrophic organisms or nem-
Scholarship Council for financial support.
atodes (Carvalhais et al., 2017; Nahar et al., 2011;
Palmer et al., 2017; Pieterse et al., 2009; Van Dam &
Oomen, 2008). In our study, the foliar JA application led to
a significant negative effect on plant biomass. This exempli- Supplementary materials
fies that hormonal signaling is costly for plants (Bald-
win, 1998; Vos, Pieterse & van Wees, 2013). Supplementary material associated with this article can be
So far, the positive role of activation of the SA pathway in found, in the online version, at doi:10.1016/j.
plant species against different microbial pathogens has been baae.2021.07.011.
reported in several species. For example,
Achuo et al. (2004)., showed that activation of the SA-sig-
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